An extensive disulfide bond network prevents tail contraction in Agrobacterium tumefaciens phage Milano
Abstract A contractile sheath and rigid tube assembly is a widespread apparatus used by bacteriophages, tailocins, and the bacterial type VI secretion system to penetrate cell membranes. In this mechanism, contraction of an external sheath powers the motion of an inner tube through the membrane. The...
| Main Authors: | , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2024-01-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-024-44959-z |
| _version_ | 1797276410693287936 |
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| author | Ravi R. Sonani Lee K. Palmer Nathaniel C. Esteves Abigail A. Horton Amanda L. Sebastian Rebecca J. Kelly Fengbin Wang Mark A. B. Kreutzberger William K. Russell Petr G. Leiman Birgit E. Scharf Edward H. Egelman |
| author_facet | Ravi R. Sonani Lee K. Palmer Nathaniel C. Esteves Abigail A. Horton Amanda L. Sebastian Rebecca J. Kelly Fengbin Wang Mark A. B. Kreutzberger William K. Russell Petr G. Leiman Birgit E. Scharf Edward H. Egelman |
| author_sort | Ravi R. Sonani |
| collection | DOAJ |
| description | Abstract A contractile sheath and rigid tube assembly is a widespread apparatus used by bacteriophages, tailocins, and the bacterial type VI secretion system to penetrate cell membranes. In this mechanism, contraction of an external sheath powers the motion of an inner tube through the membrane. The structure, energetics, and mechanism of the machinery imply rigidity and straightness. The contractile tail of Agrobacterium tumefaciens bacteriophage Milano is flexible and bent to varying degrees, which sets it apart from other contractile tail-like systems. Here, we report structures of the Milano tail including the sheath-tube complex, baseplate, and putative receptor-binding proteins. The flexible-to-rigid transformation of the Milano tail upon contraction can be explained by unique electrostatic properties of the tail tube and sheath. All components of the Milano tail, including sheath subunits, are crosslinked by disulfides, some of which must be reduced for contraction to occur. The putative receptor-binding complex of Milano contains a tailspike, a tail fiber, and at least two small proteins that form a garland around the distal ends of the tailspikes and tail fibers. Despite being flagellotropic, Milano lacks thread-like tail filaments that can wrap around the flagellum, and is thus likely to employ a different binding mechanism. |
| first_indexed | 2024-03-07T15:27:55Z |
| format | Article |
| id | doaj.art-8ffa8b55ddc8423ca2316eb1e94a3daa |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-07T15:27:55Z |
| publishDate | 2024-01-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-8ffa8b55ddc8423ca2316eb1e94a3daa2024-03-05T16:35:45ZengNature PortfolioNature Communications2041-17232024-01-0115111510.1038/s41467-024-44959-zAn extensive disulfide bond network prevents tail contraction in Agrobacterium tumefaciens phage MilanoRavi R. Sonani0Lee K. Palmer1Nathaniel C. Esteves2Abigail A. Horton3Amanda L. Sebastian4Rebecca J. Kelly5Fengbin Wang6Mark A. B. Kreutzberger7William K. Russell8Petr G. Leiman9Birgit E. Scharf10Edward H. Egelman11Department of Biochemistry and Molecular Genetics, University of Virginia School of MedicineMass Spectrometry Facility, University of Texas Medical BranchDepartment of Biological Sciences, Virginia TechDepartment of Biological Sciences, Virginia TechDepartment of Biological Sciences, Virginia TechDepartment of Biological Sciences, Virginia TechDepartment of Biochemistry and Molecular Genetics, University of Virginia School of MedicineDepartment of Biochemistry and Molecular Genetics, University of Virginia School of MedicineMass Spectrometry Facility, University of Texas Medical BranchDepartment of Biochemistry and Molecular Biology, University of Texas Medical BranchDepartment of Biological Sciences, Virginia TechDepartment of Biochemistry and Molecular Genetics, University of Virginia School of MedicineAbstract A contractile sheath and rigid tube assembly is a widespread apparatus used by bacteriophages, tailocins, and the bacterial type VI secretion system to penetrate cell membranes. In this mechanism, contraction of an external sheath powers the motion of an inner tube through the membrane. The structure, energetics, and mechanism of the machinery imply rigidity and straightness. The contractile tail of Agrobacterium tumefaciens bacteriophage Milano is flexible and bent to varying degrees, which sets it apart from other contractile tail-like systems. Here, we report structures of the Milano tail including the sheath-tube complex, baseplate, and putative receptor-binding proteins. The flexible-to-rigid transformation of the Milano tail upon contraction can be explained by unique electrostatic properties of the tail tube and sheath. All components of the Milano tail, including sheath subunits, are crosslinked by disulfides, some of which must be reduced for contraction to occur. The putative receptor-binding complex of Milano contains a tailspike, a tail fiber, and at least two small proteins that form a garland around the distal ends of the tailspikes and tail fibers. Despite being flagellotropic, Milano lacks thread-like tail filaments that can wrap around the flagellum, and is thus likely to employ a different binding mechanism.https://doi.org/10.1038/s41467-024-44959-z |
| spellingShingle | Ravi R. Sonani Lee K. Palmer Nathaniel C. Esteves Abigail A. Horton Amanda L. Sebastian Rebecca J. Kelly Fengbin Wang Mark A. B. Kreutzberger William K. Russell Petr G. Leiman Birgit E. Scharf Edward H. Egelman An extensive disulfide bond network prevents tail contraction in Agrobacterium tumefaciens phage Milano Nature Communications |
| title | An extensive disulfide bond network prevents tail contraction in Agrobacterium tumefaciens phage Milano |
| title_full | An extensive disulfide bond network prevents tail contraction in Agrobacterium tumefaciens phage Milano |
| title_fullStr | An extensive disulfide bond network prevents tail contraction in Agrobacterium tumefaciens phage Milano |
| title_full_unstemmed | An extensive disulfide bond network prevents tail contraction in Agrobacterium tumefaciens phage Milano |
| title_short | An extensive disulfide bond network prevents tail contraction in Agrobacterium tumefaciens phage Milano |
| title_sort | extensive disulfide bond network prevents tail contraction in agrobacterium tumefaciens phage milano |
| url | https://doi.org/10.1038/s41467-024-44959-z |
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